Beyond the FFA: The role of the ventral anterior temporal lobes in face processing

Highlights

• We review research implicating the vATLs in face perception and memory.

• We discuss an emerging body of research showing that a portion of the vATLs is selective for faces.

• We discuss the human and nonhuman primate face-processing system.

• The vATLs may be critically involved in congenital prosopagnosia.

• The human anterior temporal face area may be located in the perirhinal cortex.

Abstract

Extensive research has supported the existence of a specialized face-processing network that is distinct from the visual processing areas used for general object recognition. The majority of this work has been aimed at characterizing the response properties of the fusiform face area (FFA) and the occipital face area (OFA), which together are thought to constitute the core network of brain areas responsible for facial identification. Although accruing evidence has shown that face-selective patches in the ventral anterior temporal lobes (vATLs) are interconnected with the FFA and OFA, and that they play a role in facial identification, the relative contribution of these brain areas to the core face-processing network has remained unarticulated. Here we review recent research critically implicating the vATLs in face perception and memory. We propose that current models of face processing should be revised such that the ventral anterior temporal lobes serve a centralized role in the visual face-processing network. We speculate that a hierarchically organized system of face processing areas extends bilaterally from the inferior occipital gyri to the vATLs, with facial representations becoming increasingly complex and abstracted from low-level perceptual features as they move forward along this network. The anterior temporal face areas may serve as the apex of this hierarchy, instantiating the final stages of face recognition. We further argue that the anterior temporal face areas are ideally suited to serve as an interface between face perception and face memory, linking perceptual representations of individual identity with person-specific semantic knowledge.

Introduction

Humans are an intrinsically social species. More sophisticated social-cognitive skills are thought to underlie human׳s advanced intelligence, our tremendous cultural advances, and the evolution of language (Dunbar and Shultz, 2007, Herrmann et al., 2007). Superior social skills in humans are driven, in part, by increased proficiency in the identification and discrimination of conspecifics. Humans are remarkably adept at face processing and have even been described as face processing “experts” as shown by extensive clinical and psychophysical research indicating that humans have specialized processes for recognizing faces that are distinct from those used for general object recognition (Farah et al., 1998, Gauthier and Tarr, 2002, Moscovitch et al., 1997). This expertise is supported by increased specialization in a number of cortical regions involved in face processing. Over a decade of neuroimaging work has characterized the neural basis of face perception and identified several nodes or ‘patches’ that preferentially respond to faces and ultimately contribute to humans׳ unique face processing proficiencies (Haxby et al., 2000, Kanwisher and Yovel, 2006).

Because there are multiple face patches, a natural question is whether there is redundancy in the code or whether any one region is critical for normal face processing abilities. Of the regions that respond to faces more than other objects, the fusiform face area (FFA), occipital face area (OFA), and posterior superior temporal sulcus (pSTS) are proposed to constitute the “core” face recognition system, whereas the ventral anterior temporal lobe (vATL) and the amygdala are part of the “extended network” for face recognition (Haxby et al., 2000, Rossion et al., 2003). This proposal has lead to the false presumption that the vATLs play a non-critical role in face processing. However several lines of evidence strongly suggest that the vATLs play a necessary role in face perception and identification. Indeed, face-processing deficits have been more reliably observed following damage to the vATLs than more posterior portions of the face-processing network (Heywood & Cowey, 1992). Furthermore, a small but emerging body of literature has shown that a region in the vATLs is selective for faces and is interconnected with the FFA and the OFA. Early imaging studies of face perception likely missed these face-selective activations in the ATLs because they used a restricted field-of-view that excluded the inferior temporal lobe from image acquisition, or because they suffered from the well known problem of imaging the ATLs: susceptibility artifacts and signal distortion due to the proximity of these regions to the nasal sinuses and ear canals (Devlin et al., 2000, Visser et al., 2010). However, recent findings of face-selective cortical areas—“face patches”—in the vATLs of monkeys have spurred fMRI researchers to optimize signal detection in the vATLs, resulting in several recent studies suggesting that functionally homologous face-processing areas may exist in the vATLs of humans (see Fig. 1a) (Avidan et al., 2014, Pinsk et al., 2009, Rajimehr et al., 2009, Tsao et al., 2008).

Here, we will review evidence suggesting that that the ventral ATLs play a critical role in face processing. We propose that a hierarchically organized system of face-selective patches extends bilaterally from the inferior occipital gyri to the vATLs and performs the visual computations necessary for accurate facial identification. As feed-forward processing proceeds along this network, facial representations become increasingly complex and abstracted from low-level perceptual features. We further speculate that a face-selective region of the vATLS, which we will refer to as the anterior temporal face area, is the apex of this hierarchy, serving to link viewpoint invariant face representations with person-specific semantic knowledge. In the following sections, we briefly review literature on the posterior face areas (OFA and FFA; see Fig. 2) in order to place our proposal in context. The remaining sections will focus on neuroimaging and neuropsychology literature implicating the vATLs in face processing, and will highlight a small but emerging body of work that has examined the response properties of a face-sensitive region within the vATLs, the anterior temporal face area (see Fig. 2 for an illustration of the brain regions mentioned in this review). Finally we will suggest additional modifications to current neural models of face processing.